Abstract

Grain amaranths tolerate stress and produce highly nutritious seeds. We have identified several (a)biotic stress-responsive genes of unknown function in Amaranthus hypochondriacus, including the so-called Ah24 gene. Ah24 was expressed in young or developing tissues; it was also strongly induced by mechanical damage, insect herbivory and methyl jasmonate and in meristems and newly emerging leaves of severely defoliated plants. Interestingly, an in silico analysis of its 1304 bp promoter region showed a predominance of regulatory boxes involved in development, but not in defense. The Ah24 cDNA encodes a predicted cytosolic protein of 164 amino acids, the localization of which was confirmed by confocal microscopy. Additional in silico analysis identified several other Ah24 homologs, present almost exclusively in plants belonging to the Caryophyllales. The possible function of this gene in planta was examined in transgenic Ah24 overexpressing Arabidopsis thaliana and Nicotiana tabacum plants. Transformed Arabidopsis showed enhanced vegetative growth and increased leaf number with no penalty in one fitness component, such as seed yield, in experimental conditions. Transgenic tobacco plants, which grew and reproduced normally, had increased insect herbivory resistance. Modified vegetative growth in transgenic Arabidopsis coincided with significant changes in the expression of genes controlling phytohormone synthesis or signaling, whereas increased resistance to insect herbivory in transgenic tobacco coincided with higher jasmonic acid and proteinase inhibitor activity levels, plus the accumulation of nicotine and several other putative defense-related metabolites. It is proposed that the primary role of the Ah24 gene in A. hypochondriacus is to contribute to a rapid recovery post-wounding or defoliation, although its participation in defense against insect herbivory is also plausible.

Highlights

  • Grain amaranths are C4 dicotyledonous plants that belong to the Amaranhaceae family and the Caryophyllales order, which groups several plant species with interesting physiological and agronomical characteristics (Stallknecht and SchulzSchaeffer, 1993; Brenner et al, 2000)

  • Ah24 Gene and Coding Region Employing PCR-based cDNA subtraction, a partial Ah24 cDNA clone of 858 bp, containing part of the 5′ UTR region, was obtained from combined cDNA libraries of grain amaranth plants subjected to water- and salt-stress, insect herbivory, and mechanical damage (Fomsgaard et al, 2010)

  • The prediction was corroborated by an 82% identity with fingerprint peptides derived from a proteomic analysis of an A. hypochondriacus protein induced by exogenous methyl jasmonate (MeJA) (Navarro-Meléndez, 2009; Figure S1 in Supplementary Materials)

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Summary

Introduction

Grain amaranths are C4 dicotyledonous plants that belong to the Amaranhaceae family and the Caryophyllales order, which groups several plant species with interesting physiological and agronomical characteristics (Stallknecht and SchulzSchaeffer, 1993; Brenner et al, 2000). Grain amaranths show exceptional tolerance to severe defoliation (CastrillónArbeláez et al, 2012; Vargas-Ortiz et al, 2013), which was found to be associated with an efficient utilization of relatively high levels of stored carbon reserves in stem and roots. They are known to readily respond to chemical elicitors of defense responses, such as jasmonic acid (JA) (Délano-Frier et al, 2004, 2011; Sánchez-Hernández et al, 2004) or benzothiadiazole (Casarrubias-Castillo et al, 2014), to increase their resistance against highly damaging sucking insect pests, such as the tarnished bug Lygus lineolaris, or against potentially lethal pathogenic bacteria

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